Comparative analysis of detoxification-related gene superfamilies across five hemipteran species
Abstract Background Hemiptera is one of the most speciose orders of insects, and the most speciose considering Hemimetabola. Through their evolutive history, hemipterans with different feeding habits have adapted to deal with different chemical challenges. Three major gene families are involved in x...
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| Format: | Article |
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BMC
2022-11-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-022-08974-y |
| _version_ | 1797984042266656768 |
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| author | Mariano Volonté Lucila Traverso Jose Manuel Latorre Estivalis Francisca Cunha Almeida Sheila Ons |
| author_facet | Mariano Volonté Lucila Traverso Jose Manuel Latorre Estivalis Francisca Cunha Almeida Sheila Ons |
| author_sort | Mariano Volonté |
| collection | DOAJ |
| description | Abstract Background Hemiptera is one of the most speciose orders of insects, and the most speciose considering Hemimetabola. Through their evolutive history, hemipterans with different feeding habits have adapted to deal with different chemical challenges. Three major gene families are involved in xenobiotic detoxification in insects: the cytochromes P450 (CYPs), carboxyl/cholinesterases (CCEs), and glutathione transferases (GSTs). Here we perform a comparative analysis on the complement of these gene superfamilies across five hemipteran species; four heteropterans (the pentatomid plant feeders Nezara viridula and Halyomorpha halys; the hematophagous Cimex lectularius, Cimicidae, and Rhodnius prolixus, Reduviidae), and one Auchenorrhyncha plant feeder (Nilaparvata lugens). Results Our results point to an expansion of several enzyme families associated with xenobiotic detoxification in heteropterans with respect to other species and the existence of a dynamic evolution pattern including CYP3 clan, hormone and pheromone processing class in the CCE superfamily, and sigma class in GST superfamily. Other detoxification-related families are reduced in the hemipteran species analyzed here: reduction or even absence of epsilon class and reduced delta class in GST superfamily; absence of mitochondrial CYP12 family; absence of CYP9 family in CYP3 clan; and reduction or even absence of some dietary/detoxification groups of CCEs. Interestingly, the most polyphagous species analyzed here (H. halys) is also the one that presents the largest repertoire of detoxification enzymes. Gene cluster analysis suggests that this could be due to gene duplication events. Conclusions The evolutionary analysis performed here reveals characteristics that are both common and particular for heteropterans. The composition and organization of detoxification-related gene families could shed light on evolutionary forces that shaped their divergence. These families are important for both the detoxification of diet products and for conferring tolerance or resistance to synthetic insecticides. Furthermore, we present the first comprehensive analysis of detoxification gene superfamilies in N. viridula, an understudied species in spite of its economic relevance as a crop pest. The information obtained is of interest for basic insect science as well as for the control of harmful species and the management of insecticide resistance. |
| first_indexed | 2024-04-11T06:55:27Z |
| format | Article |
| id | doaj.art-325a94d62cc94751afde15785d646ad1 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-11T06:55:27Z |
| publishDate | 2022-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-325a94d62cc94751afde15785d646ad12022-12-22T04:39:02ZengBMCBMC Genomics1471-21642022-11-0123111710.1186/s12864-022-08974-yComparative analysis of detoxification-related gene superfamilies across five hemipteran speciesMariano Volonté0Lucila Traverso1Jose Manuel Latorre Estivalis2Francisca Cunha Almeida3Sheila Ons4Laboratorio de Neurobiología de Insectos (LNI), Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, CENEXA, CONICETLaboratorio de Neurobiología de Insectos (LNI), Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, CENEXA, CONICETLaboratorio de Insectos Sociales, Instituto de Fisiología, Biología Molecular y Neurociencias, Universidad de Buenos Aires – CONICETGrupo de Investigación en Filogeografía y Filogenias Moleculares, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos AiresLaboratorio de Neurobiología de Insectos (LNI), Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, CENEXA, CONICETAbstract Background Hemiptera is one of the most speciose orders of insects, and the most speciose considering Hemimetabola. Through their evolutive history, hemipterans with different feeding habits have adapted to deal with different chemical challenges. Three major gene families are involved in xenobiotic detoxification in insects: the cytochromes P450 (CYPs), carboxyl/cholinesterases (CCEs), and glutathione transferases (GSTs). Here we perform a comparative analysis on the complement of these gene superfamilies across five hemipteran species; four heteropterans (the pentatomid plant feeders Nezara viridula and Halyomorpha halys; the hematophagous Cimex lectularius, Cimicidae, and Rhodnius prolixus, Reduviidae), and one Auchenorrhyncha plant feeder (Nilaparvata lugens). Results Our results point to an expansion of several enzyme families associated with xenobiotic detoxification in heteropterans with respect to other species and the existence of a dynamic evolution pattern including CYP3 clan, hormone and pheromone processing class in the CCE superfamily, and sigma class in GST superfamily. Other detoxification-related families are reduced in the hemipteran species analyzed here: reduction or even absence of epsilon class and reduced delta class in GST superfamily; absence of mitochondrial CYP12 family; absence of CYP9 family in CYP3 clan; and reduction or even absence of some dietary/detoxification groups of CCEs. Interestingly, the most polyphagous species analyzed here (H. halys) is also the one that presents the largest repertoire of detoxification enzymes. Gene cluster analysis suggests that this could be due to gene duplication events. Conclusions The evolutionary analysis performed here reveals characteristics that are both common and particular for heteropterans. The composition and organization of detoxification-related gene families could shed light on evolutionary forces that shaped their divergence. These families are important for both the detoxification of diet products and for conferring tolerance or resistance to synthetic insecticides. Furthermore, we present the first comprehensive analysis of detoxification gene superfamilies in N. viridula, an understudied species in spite of its economic relevance as a crop pest. The information obtained is of interest for basic insect science as well as for the control of harmful species and the management of insecticide resistance.https://doi.org/10.1186/s12864-022-08974-yGlutathione transferasesCytochromes P450Carboxyl/cholinesterasesInsectsPentatomidTriatomine |
| spellingShingle | Mariano Volonté Lucila Traverso Jose Manuel Latorre Estivalis Francisca Cunha Almeida Sheila Ons Comparative analysis of detoxification-related gene superfamilies across five hemipteran species BMC Genomics Glutathione transferases Cytochromes P450 Carboxyl/cholinesterases Insects Pentatomid Triatomine |
| title | Comparative analysis of detoxification-related gene superfamilies across five hemipteran species |
| title_full | Comparative analysis of detoxification-related gene superfamilies across five hemipteran species |
| title_fullStr | Comparative analysis of detoxification-related gene superfamilies across five hemipteran species |
| title_full_unstemmed | Comparative analysis of detoxification-related gene superfamilies across five hemipteran species |
| title_short | Comparative analysis of detoxification-related gene superfamilies across five hemipteran species |
| title_sort | comparative analysis of detoxification related gene superfamilies across five hemipteran species |
| topic | Glutathione transferases Cytochromes P450 Carboxyl/cholinesterases Insects Pentatomid Triatomine |
| url | https://doi.org/10.1186/s12864-022-08974-y |
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